#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Multiple Plant Surface Signals are Sensed by Different Mechanisms in the Rice Blast Fungus for Appressorium Formation


Surface recognition and penetration are among the most critical plant infection processes in foliar pathogens. In Magnaporthe oryzae, the Pmk1 MAP kinase regulates appressorium formation and penetration. Its orthologs also are known to be required for various plant infection processes in other phytopathogenic fungi. Although a number of upstream components of this important pathway have been characterized, the upstream sensors for surface signals have not been well characterized. Pmk1 is orthologous to Kss1 in yeast that functions downstream from Msb2 and Sho1 for filamentous growth. Because of the conserved nature of the Pmk1 and Kss1 pathways and reduced expression of MoMSB2 in the pmk1 mutant, in this study we functionally characterized the MoMSB2 and MoSHO1 genes. Whereas the Momsb2 mutant was significantly reduced in appressorium formation and virulence, the Mosho1 mutant was only slightly reduced. The Mosho1 Momsb2 double mutant rarely formed appressoria on artificial hydrophobic surfaces, had a reduced Pmk1 phosphorylation level, and was nonresponsive to cutin monomers. However, it still formed appressoria and caused rare, restricted lesions on rice leaves. On artificial hydrophilic surfaces, leaf surface waxes and primary alcohols-but not paraffin waxes and alkanes- stimulated appressorium formation in the Mosho1 Momsb2 mutant, but more efficiently in the Momsb2 mutant. Furthermore, expression of a dominant active MST7 allele partially suppressed the defects of the Momsb2 mutant. These results indicate that, besides surface hydrophobicity and cutin monomers, primary alcohols, a major component of epicuticular leaf waxes in grasses, are recognized by M. oryzae as signals for appressorium formation. Our data also suggest that MoMsb2 and MoSho1 may have overlapping functions in recognizing various surface signals for Pmk1 activation and appressorium formation. While MoMsb2 is critical for sensing surface hydrophobicity and cutin monomers, MoSho1 may play a more important role in recognizing rice leaf waxes.


Vyšlo v časopise: Multiple Plant Surface Signals are Sensed by Different Mechanisms in the Rice Blast Fungus for Appressorium Formation. PLoS Pathog 7(1): e32767. doi:10.1371/journal.ppat.1001261
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001261

Souhrn

Surface recognition and penetration are among the most critical plant infection processes in foliar pathogens. In Magnaporthe oryzae, the Pmk1 MAP kinase regulates appressorium formation and penetration. Its orthologs also are known to be required for various plant infection processes in other phytopathogenic fungi. Although a number of upstream components of this important pathway have been characterized, the upstream sensors for surface signals have not been well characterized. Pmk1 is orthologous to Kss1 in yeast that functions downstream from Msb2 and Sho1 for filamentous growth. Because of the conserved nature of the Pmk1 and Kss1 pathways and reduced expression of MoMSB2 in the pmk1 mutant, in this study we functionally characterized the MoMSB2 and MoSHO1 genes. Whereas the Momsb2 mutant was significantly reduced in appressorium formation and virulence, the Mosho1 mutant was only slightly reduced. The Mosho1 Momsb2 double mutant rarely formed appressoria on artificial hydrophobic surfaces, had a reduced Pmk1 phosphorylation level, and was nonresponsive to cutin monomers. However, it still formed appressoria and caused rare, restricted lesions on rice leaves. On artificial hydrophilic surfaces, leaf surface waxes and primary alcohols-but not paraffin waxes and alkanes- stimulated appressorium formation in the Mosho1 Momsb2 mutant, but more efficiently in the Momsb2 mutant. Furthermore, expression of a dominant active MST7 allele partially suppressed the defects of the Momsb2 mutant. These results indicate that, besides surface hydrophobicity and cutin monomers, primary alcohols, a major component of epicuticular leaf waxes in grasses, are recognized by M. oryzae as signals for appressorium formation. Our data also suggest that MoMsb2 and MoSho1 may have overlapping functions in recognizing various surface signals for Pmk1 activation and appressorium formation. While MoMsb2 is critical for sensing surface hydrophobicity and cutin monomers, MoSho1 may play a more important role in recognizing rice leaf waxes.


Zdroje

1. ValentB

ChumleyFG

1991 Molecular genetic analysis of the rice blast fungus Magnaporthe grisea. Annu Rev Phytopathol 29 443 467

2. XuJR

PengYL

DickmanMB

SharonA

2006 The dawn of fungal pathogen genomics. Annu Rev Phytopathol 44 337 366

3. WilsonRA

TalbotNJ

2009 Under pressure: investigating the biology of plant infection by Magnaporthe oryzae. Nature Rev Micriobiol 7 185 195

4. KankanalaP

CzymmekK

ValentB

2007 Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19 706 724

5. ChoiWB

DeanRA

1997 The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9 1973 1983

6. MitchellTK

DeanRA

1995 The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7 1869 1878

7. UchiyamaT

OkuyamaK

1990 Participation of Oryza-Sativa leaf wax in appressorium formation by Pyricularia oryzae. Phytochemistry 29 91 92

8. XiaoJZ

WatanabeT

SekidoS

ChoiWB

KamakuraT

1997 An anti-hydrotactic response and solid surface recognition of germ tubes of the rice blast fungus, Magnaporthe grisea. Biosci Biotechnol Biochem 61 1225 1229

9. OhtakeM

YamamotoH

UchiyamaT

1999 Influences of metabolic inhibitors and hydrolytic enzymes on the adhesion of appressoria of Pyricularia oryzae to wax-coated cover-glasses. Biosci Biotechnol Biochem 63 978 982

10. JelittoTC

PageHA

ReadND

1994 Role of external signals in regulating the pre-penetration phase of infection by the rice blast fungus Magnaporthe grisea. Planta 194 471 477

11. LiuH

SureshA

WillardFS

SiderovskiDP

LuS

2007 Rgs1 regulates multiple G alpha subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism. Embo Journal 26 690 700

12. ZhaoX

MehrabiR

XuJ-R

2007 Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6 1701 1714

13. ChenRE

ThornerJ

2007 Function and regulation in MAPK signaling pathways: Lessons learned from the yeast Saccharomyces cerevisiae. Bioch Biophys Acta 1773 1311 1340

14. ZhaoXH

KimY

ParkG

XuJR

2005 A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17 1317 1329

15. ParkG

XueC

ZhaoX

KimY

OrbachM

2006 Multiple upstream signals converge on an adaptor protein Mst50 to activate the PMK1 pathway in Magnaporthe grisea. Plant Cell 18 2822 2835

16. ParkG

XueGY

ZhengL

LamS

XuJR

2002 MST12 regulates infectious growth but not appressorium formation in the rice blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 15 183 192

17. KramerB

ThinesE

FosterAJ

2009 MAP kinase signalling pathway components and targets conserved between the distantly related plant pathogenic fungi Mycosphaerella graminicola and Magnaporthe grisea. Fungal Genet Biol 46 667 681

18. RispailN

SoanesDM

AntC

CzajkowskiR

GrünlerA

2009 Comparative genomics of MAP kinase and calcium–calcineurin signalling components in plant and human pathogenic fungi. Fung Genet Biol 46 287 298

19. DeZwaanTM

CarrollAM

ValentB

SweigardJA

1999 Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11 2013 2030

20. BardwellL

2006 Mechanisms of MAPK signalling specificity. Biochem Soc Transact 34 837 841

21. CullenPJ

SchultzJ

HoreckaJ

StevensonBJ

JigamiY

2000 Defects in protein glycosylation cause SHO1-dependent activation of a STE12 signaling pathway in yeast. Genetics 155 1005 1018

22. PitoniakA

BirkayaB

DionneHM

VadaieN

CullenPJ

2009 The signaling mucins Msb2 and Hkr1 differentially regulate the filamentation mitogen-activated protein kinase pathway and contribute to a multimodal response. Mol Biol Cell 20 3101 3114

23. RaittDC

PosasF

SaitoH

2000 Yeast Cdc42 GTPase and Ste20 PAK-like kinase regulate Sho1-dependent activation of the Hog1 MAPK pathway. EMBO J 19 4623 4631

24. LanverD

Mendoza-MendozaA

BrachmannA

KahmannR

2010 Sho1 and Msb2-related proteins regulate appressorium development in the smut fungus Ustilago maydis. Plant Cell 22 2085 2101

25. MadhaniHD

FinkGR

1997 Combinatorial control required for the specificity of yeast MAPK signaling. Science 275 1314 1317

26. VillalbaF

CollemareJ

LandraudP

LambouK

BrozekV

2008 Improved gene targeting in Magnaporthe grisea by inactivation of MgKU80 required for non-homologous end joining. Fungal Genet Biol 45 68 75

27. GilbertRD

JohnsonAM

DeanRA

1996 Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol Mol Plant Pathol 48 335 346

28. KunstL

SamuelsAL

2003 Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42 51 80

29. YuD

RanathungeK

HuangH

PeiZ

FrankeR

2008 Wax Crystal-Sparse Leaf1 encodes a beta-ketoacyl CoA synthase involved in biosynthesis of cuticular waxes on rice leaf. Planta 228 675 685

30. DixonKP

XuJR

SmirnoffN

TalbotNJ

1999 Independent signaling pathways regulate cellular turgor during hyperosmotic stress and appressorium-mediated plant infection by Magnaporthe grisea. Plant Cell 11 2045 2058

31. HattrupCL

GendlerSJ

2008 Structure and function of the cell surface (tethered) mucins. Annu Rev Physiol 70 431 457

32. CullenPJ

SabbaghWJr

GrahamE

IrickMM

van OldenEK

2004 A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18 1695 1708

33. TatebayashiK

TanakaK

YangHY

YamamotoK

MatsushitaY

2007 Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26 3521 3533

34. KamakuraT

YamaguchiS

SaitohK

TeraokaT

YamaguchiI

2002 A novel gene, CBP1, encoding a putative extracellular chitin- binding protein, may play an important role in the hydrophobic surface sensing of Magnaporthe grisea during appressorium differentiation. Mol Plant-Microbe Interact 15 437 444

35. ZabkaV

StanglM

BringmannG

VoggG

RiedererM

2008 Host surface properties affect prepenetration processes in the barley powdery mildew fungus. New Phytol 177 251 263

36. XuJR

HamerJE

1996 MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10 2696 2706

37. VadaieN

DionneH

AkajagborDS

NickersonSR

KrysanDJ

2008 Cleavage of the signaling mucin Msb2 by the aspartyl protease Yps1 is required for MAPK activation in yeast. J Cell Biol 181 1073 1081

38. TalbotNJ

EbboleDJ

HamerJE

1993 Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5 1575 1590

39. SweigardJA

CarrollAM

FarrallL

ChumleyFG

ValentB

1998 Magnaporthe grisea pathogenicity genes obtained through insertional mutagenesis. Mol Plant-Microbe Interact 11 404 412

40. XueCY

ParkG

ChoiWB

ZhengL

DeanRA

2002 Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell 14 2107 2119

41. SweigardJA

ChumleyFG

ValentB

1992 Disruption of a Magnaporthe grisea cutinase gene. Mol Gen Genet 232 183 190

42. BrunoKS

TenjoF

LiL

HamerJE

XuJR

2004 Cellular localization and role of kinase activity of PMK1 in Magnaporthe grisea. Eukaryot Cell 3 1525 1532

43. LiuWD

XieSY

ZhaoXH

ChenX

ZhengWH

2010 A homeobox gene is essential for conidiogenesis of the rice blast fungus Magnaporthe oryzae. Mol Plant-Microbe Interact 23 366 375

44. BourettTM

SweigardJA

CzymmekKJ

CarrollA

HowardRJ

2002 Reef coral fluorescent proteins for visualizing fungal pathogens. Fungal Genet Biol 37 211 220

45. CullenPJ

SabbaghW

GrahamE

IrickMM

van OldenEK

2004 A signaling mucin at the head of the Cdc42- and MAPK-dependent filamentous growth pathway in yeast. Genes Dev 18 1695 1708

46. ZarrinparA

BhattacharyyaRP

NittlerMP

LimWA

2004 Sho1 and Pbs2 act as coscaffolds linking components in the yeast high osmolarity MAP kinase pathway. Mol Cell 14 825 832

47. TuckerSL

ThorntonCR

TaskerK

JacobC

GilesG

2004 A fungal metallothionein is required for pathogenicity of Magnaporthe grisea. Plant Cell 16 1575 1588

48. KogaH

1994 Hypersensitive death, autofluorescence, and ultrastructural-changes in cells of leaf sheaths of susceptible and resistant near-isogenic lines of rice (PI-Z(T)) in relation to penetration and growth of Pycularia oryza. Can J Bot 72 1463 1477

49. ParkG

BrunoKS

StaigerCJ

TalbotNJ

XuJR

2004 Independent genetic mechanisms mediate turgor generation and penetration peg formation during plant infection in the rice blast fungus. Mol Microbiol 53 1695 1707

50. LiL

XueCY

BrunoK

NishimuraM

XuJR

2004 Two PAK kinase genes, CHM1 and MST20, have distinct functions in Magnaporthe grisea. Mol Plant-Microbe Interact 17 547 556

51. TalbotNJ

KershawMJ

WakleyGE

deVriesOMH

WesselsJGH

1996 MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8 985 999

52. ChenXB

GoodwinSM

BoroffVL

LiuXL

JenksMA

2003 Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15 1170 1185

53. LiL

DingSL

SharonA

OrbachM

XuJR

2007 Mir1 is highly upregulated and localized to nuclei during infectious hyphal growth in the rice blast fungus. Mol Plant-Microbe Interact 20 448 458

54. LivakKJ

SchmittgenTD

2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25 402 408

55. DingS

LiuW

LLiukA

RibotC

ValletJ

2010 The Tig1 HDAC complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22 2495 2508

56. SambrookJ

RussellD

2001 Molecular Cloning - A Laboratory Manual Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#